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Prognostic effects of causative virus in hepatocellular carcinoma according to the Japan integrated staging (JIS) score

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Abstract

Background

The Japan integrated staging (JIS) score is recognized to be useful in managing hepatocellular carcinoma (HCC). We evaluated the effects of the causative virus in patients stratified by this system.

Methods

We compared clinicopathologic features, cumulative and tumor-free survival rates, and causes of death between 301 hepatitis C virus-positive patients (HCV group) and 60 hepatitis B virus-positive patients (HBV group).

Results

Among patients with low JIS scores (0 or 1), the proportions of patients with high aspartate and alanine aminotranferase activities, moderate-to-severe active hepatitis, and with cirrhosis were significantly higher in the HCV than in the HBV group. Among patients with high JIS scores (2 to 4), the proportion with moderate-to-severe active hepatitis was also significantly higher in the HCV group. In patients with low JIS scores, those in the HCV group had significantly lower tumor-free and cumulative survival rates than those in the HBV group. Although no patient in the HBV group died of causes other than liver disease (HCC or hepatic failure), some patients in the HCV group died of causes other than liver disease. The proportion of patients who died because of HCC recurrence tended to be higher among patients with high JIS scores than among patients with a low JIS score.

Conclusions

The effects of viral status on survival outcomes are greatest in patients with JIS scores of 0 or 1.

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References

  1. InstitutionalAuthorNameThe Cancer of the Liver Italian Program (CLIP) Investigators (1998) ArticleTitleA new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients Hepatology 28 751–5

    Google Scholar 

  2. InstitutionalAuthorNameCLIP Group (Cancer of the Liver Italian Program) (1998) ArticleTitleTamoxifen in treatment of hepatocellular carcinoma: a randomised controlled trial Lancet 352 17–20

    Google Scholar 

  3. InstitutionalAuthorNameThe Cancer of the Liver Italian Program (CLIP) Investigators (2000) ArticleTitleProspective validation of the CLIP score: a new prognostic system for patients with cirrhosis and hepatocellular carcinoma Hepatology 31 840–5

    Google Scholar 

  4. JM Llovet J Bruix (2000) ArticleTitleBCLC group. Prospective validation of the Cancer of the Liver Italian Program (CLIP) score: a new prognostic system for patients with cirrhosis and hepatocellular carcinoma: correspondence Hepatology 32 679–80 Occurrence Handle10.1053/jhep.2000.16475 Occurrence Handle10991637

    Article  PubMed  Google Scholar 

  5. F Farinati M Rinaldi S Gianni R Naccarato (2000) ArticleTitleHow should patients with hepatocellular carcinoma be staged? Validation of a new prognostic system Cancer 89 2266–73 Occurrence Handle10.1002/1097-0142(20001201)89:11<2266::AID-CNCR15>3.0.CO;2-0 Occurrence Handle11147597

    Article  PubMed  Google Scholar 

  6. S Ueno G Tanabe K Sako T Hiwaki H Hokotate Y Fukukura et al. (2001) ArticleTitleDiscrimination value of the new western prognostic system (CLIP score) for hepatocellular carcinoma in 662 Japanese patients Hepatology 23 529–34 Occurrence Handle10.1053/jhep.2001.27219

    Article  Google Scholar 

  7. I Levy M Sherman InstitutionalAuthorNameThe Liver Cancer Study Group of the University of Toronto (2002) ArticleTitleStaging of hepatocellular carcinoma: assessment of the CLIP, Okuda, and Child-Pugh staging systems in a cohort of 257 patients in Toronto Gut 50 881–5 Occurrence Handle10.1136/gut.50.6.881 Occurrence Handle12010894

    Article  PubMed  Google Scholar 

  8. C Rabe M Lenz V Schmitz T Pilz R Fimmers T Sauerbruch et al. (2003) ArticleTitleAn independent evaluation of modern prognostic scores in a central European cohort of 120 patients with hepatocellular carcinoma Eur J Gastroenterol Hepatol 15 1305–15 Occurrence Handle10.1097/00042737-200312000-00009 Occurrence Handle14624154

    Article  PubMed  Google Scholar 

  9. E Giannini D Risso F Botta P Romagnoli F Malfatti A Fumagalli et al. (2004) ArticleTitlePrognosis of hepatocellular carcinoma in anti-HCV positive cirrhotic patients: a single-centre comparison among four different staging systems J Intern Med 225 399–408 Occurrence Handle10.1046/j.1365-2796.2003.01284.x

    Article  Google Scholar 

  10. S Wildi BC Pestalozzi L McCormack PA Clavien (2004) ArticleTitleCritical evaluation of the different staging systems for hepatocellular carcinoma Br J Surg 91 400–8 Occurrence Handle10.1002/bjs.4554 Occurrence Handle15048738

    Article  PubMed  Google Scholar 

  11. M Kudo H Chung Y Osaki (2003) ArticleTitlePrognostic staging system for hepatocellular carcinoma (CLIP score): its value and limitations, and a proposal for a new staging system, the Japan integrated staging score (JIS score) J Gastroenterol 38 207–15 Occurrence Handle10.1007/s005350300038 Occurrence Handle12673442

    Article  PubMed  Google Scholar 

  12. InstitutionalAuthorNameLiver Cancer Study Group of Japan (2000) The general rules for the clinical and pathological study of primary liver cancer (in Japanese) EditionNumber4th ed. Kanehara Tokyo 19

    Google Scholar 

  13. M Kudo H Chung S Haji Y Osaki H Oka T Seki et al. (2004) ArticleTitleValidation of a new prognostic staging system for hepatocellular carcinoma: the JIS score compared with the CLIP score Hepatology 40 1396–405 Occurrence Handle10.1002/hep.20486 Occurrence Handle15565571

    Article  PubMed  Google Scholar 

  14. Y Shiratori S Shiina M Imamura M Kato F Kanai T Okudaira et al. (1995) ArticleTitleCharacteristic difference of hepatocellular carcinoma between hepatitis B- and C-viral infection in Japan Hepatology 22 1027–33 Occurrence Handle10.1016/0270-9139(95)90605-3 Occurrence Handle7557847

    Article  PubMed  Google Scholar 

  15. S Miyagawa S Kawasaki M Makuuchi (1996) ArticleTitleComparison of the characteristics of hepatocellular carcinoma between hepatitis B and C viral infection: tumor multicentricity in cirrhotic liver with hepatitis C Hepatology 24 307–10 Occurrence Handle8690397

    PubMed  Google Scholar 

  16. H Tanizaki M Ryu T Kinoshita N Kawano M Konishi A Cho et al. (1997) ArticleTitleComparison of clinical features and survival in patients with hepatitis B and C virus-related hepatocellular carcinoma Jpn J Clin Oncol 27 67–70 Occurrence Handle10.1093/jjco/27.2.67 Occurrence Handle9152792

    Article  PubMed  Google Scholar 

  17. N Yamanaka T Tanaka W Tanaka J Yamanaka C Yasui N Kuroda et al. (1997) ArticleTitleCorrelation of hepatitis virus serologic status with clinicopathologic features in patients undergoing hepatectomy for hepatocellular carcinoma Cancer 79 1509–15 Occurrence Handle10.1002/(SICI)1097-0142(19970415)79:8<1509::AID-CNCR10>3.0.CO;2-1 Occurrence Handle9118031

    Article  PubMed  Google Scholar 

  18. T Shuto K Hirohashi S Kubo T Taukamoto T Yamamoto K Wakasa et al. (1998) ArticleTitleDifferences of resected hepatocellular carcinoma with hepatitis B or C virus Hepatogastroenterology 45 1722–5 Occurrence Handle9840135

    PubMed  Google Scholar 

  19. S Roayaie M Ben Haim S Emre TM Fishbein PA Sheiner CM Miller et al. (2000) ArticleTitleComparison of surgical outcomes for hepatocellular carcinoma in patients with hepatitis B versus hepatitis C: a western experience Ann Surg Oncol 7 764–70 Occurrence Handle10.1007/s10434-000-0764-8 Occurrence Handle11129425

    Article  PubMed  Google Scholar 

  20. N Iizuka M Oka H Yamada-Okabe N Mori T Tamesa T Okada et al. (2002) ArticleTitleComparison of gene expression profiles between hepatitis B virus- and hepatitis C virus-infected hepatocellular carcinoma by oligonucleotide microarray data on the basis of a supervised learning method Cancer Res 62 3939–44 Occurrence Handle12124323

    PubMed  Google Scholar 

  21. HA Edmondson PE Steiner (1954) ArticleTitlePrimary carcinoma of the liver: a study of 100 cases among 48 900 necropsies Cancer 7 462–503 Occurrence Handle13160935

    PubMed  Google Scholar 

  22. InstitutionalAuthorNameLiver Cancer Study Group of Japan (1997) Classification of ordinary liver cancer EditionNumberFirst English ed. Kanehara Tokyo

    Google Scholar 

  23. VJ Desmet M Gerber JH Hoofnagle M Manns PJ Scheuer (1994) ArticleTitleClassicification of chronic hepatitis: diagnosis, grading and staging Hepatology 19 1513–20 Occurrence Handle10.1016/0270-9139(94)90250-X Occurrence Handle8188183

    Article  PubMed  Google Scholar 

  24. T Shuto H Kinoshita K Hirohashi S Kubo H Tanaka T Tsukamoto et al. (1996) ArticleTitleIndications for, and effectiveness of, a second hepatic resection for recurrent hepatocellular carcinoma Hepatogastroenterology 43 932–7 Occurrence Handle8884316

    PubMed  Google Scholar 

  25. Liver Cancer (1990) ArticleTitleStudy Group of Japan. Primary liver cancer in Japan: clinicopathological features and results of surgical treatment Ann Surg 221 277–87

    Google Scholar 

  26. T Kumada S Nakano I Takeda K Sugiyama T Osada S Kiriyama et al. (1997) ArticleTitlePatterns of recurrence after initial treatment in patients with small hepatocellular carcinoma Hepatology 25 87–92 Occurrence Handle8985270

    PubMed  Google Scholar 

  27. M Sakon K Umeshita H Nagano H Eguchi S Kishimoto A Miyamoto et al. (2000) ArticleTitleClinical significance of hepatic resection in hepatocellular carcinoma: analysis by disease-free survival curves Arch Surg 135 1456–9 Occurrence Handle10.1001/archsurg.135.12.1456 Occurrence Handle11115352

    Article  PubMed  Google Scholar 

  28. K Ikeda S Saitoh I Koida Y Arase A Tsubota K Chayama et al. (1993) ArticleTitleA multivariate analysis of risk factors for hepatocellular carcinogenesis: a prospective observation of 795 patients with viral and alcoholic cirrhosis Hepatology 18 47–53 Occurrence Handle10.1016/0270-9139(93)90505-H Occurrence Handle7686879

    Article  PubMed  Google Scholar 

  29. S Takano O Yokosuka F Imazeki M Tagawa M Omata (1995) ArticleTitleIncidence of hepatocellular carcinoma in chronic hepatitis B and C: a prospective study of 251 patients Hepatology 21 650–5 Occurrence Handle10.1016/0270-9139(95)90513-8 Occurrence Handle7875662

    Article  PubMed  Google Scholar 

  30. S Kubo S Nishiguchi K Hirohashi T Shuto T Kuroki S Minamitani et al. (1998) ArticleTitleClinicopathological criteria for multicentricity of hepatocellular carcinoma and risk factors for such carcinogenesis Jpn J Cancer Res 89 419–26 Occurrence Handle9617348

    PubMed  Google Scholar 

  31. S Kubo S Nishiguchi T Shuto H Tanaka T Tsukamoto K Hirohashi et al. (1999) ArticleTitleEffects of continuous hepatitis with persistent hepatitis C viremia on outcome after resection of hepatocellular carcinoma Jpn J Cancer Res 90 162–70 Occurrence Handle10189886

    PubMed  Google Scholar 

  32. S Kubo H Kinoshita K Hirohashi H Tanaka T Tsukamoto H Hamba et al. (1999) ArticleTitlePatterns and risk factors for recurrence after liver resection for well-differentiated hepatocellular carcinoma; a special reference to multicentric carcinogenesis after operation Hepatogastroenterology 46 3212–5 Occurrence Handle10626188

    PubMed  Google Scholar 

  33. S Kubo K Hirohashi H Tanaka T Tsukamoto T Shuto T Yamamoto et al. (2000) ArticleTitleEffect of viral status on recurrence after liver resection for patients with hepatitis B virus-related hepatocellular carcinoma Cancer 88 1016–24 Occurrence Handle10.1002/(SICI)1097-0142(20000301)88:5<1016::AID-CNCR10>3.0.CO;2-V Occurrence Handle10699889

    Article  PubMed  Google Scholar 

  34. S Kubo K Hirohashi H Tanaka T Tsukamoto T Shuto I Higaki et al. (2001) ArticleTitleVirologic and biochemical changes and prognosis after liver resection for hepatitis B virus-related hepatocellular carcinoma Dig Surg 18 26–33 Occurrence Handle10.1159/000050093 Occurrence Handle11244256

    Article  PubMed  Google Scholar 

  35. S Ko Y Nakajima H Kanehiro M Hisanaga Y Aomatsu T Kin et al. (1996) ArticleTitleSignificant influence of accompanying chronic hepatitis status on recurrence of hepatocellular carcinoma after hepatectomy: result of multivariate analysis Ann Surg 224 591–5 Occurrence Handle10.1097/00000658-199611000-00001 Occurrence Handle8916872

    Article  PubMed  Google Scholar 

  36. K Shirabe K Takenaka A Taketomi N Kawahara K Yamamoto M Shimada et al. (1996) ArticleTitlePostoperative hepatitis status as a significant risk factor for recurrence in cirrhotic patients with small hepatocellular carcinoma Cancer 77 1050–5 Occurrence Handle10.1002/(SICI)1097-0142(19960315)77:6<1050::AID-CNCR7>3.0.CO;2-L Occurrence Handle8635122

    Article  PubMed  Google Scholar 

  37. K Tarao A Takemiya S Tamai Y Sugimasa S Ohkawa M Akaike et al. (1997) ArticleTitleRelationship between the recurrence of hepatocellular carcinoma (HCC) and serum alanine aminotransferase levels in hepatectomized patients with hepatitis C virus-associated cirrhosis and HCC Cancer 79 688–94 Occurrence Handle10.1002/(SICI)1097-0142(19970215)79:4<688::AID-CNCR5>3.0.CO;2-A Occurrence Handle9024706

    Article  PubMed  Google Scholar 

  38. S Kubo T Yamamoto T Ikebe T Shuto K Hirohashi H Tanaka et al. (1999) ArticleTitleRelationship between multicentric occurrence of hepatocellular carcinoma and histology of noncancerous hepatic tissue in patients with chronic hepatitis C Jpn J Cancer Res 90 1076–80 Occurrence Handle10595735

    PubMed  Google Scholar 

  39. H Yoshida Y Shiratori M Moriyama Y Arakawa T Ide M Sata et al. (1999) ArticleTitleInterferon therapy reduces the risk of hepatocellular carcinoma: national surveillance program of cirrhotic and noncirrhotic patients with chronic hepatitis C in Japan Ann Intern Med 131 174–81 Occurrence Handle10428733

    PubMed  Google Scholar 

  40. S Kubo K Hirohashi H Tanaka T Tsukamoto T Shuto T Ikebe et al. (2000) ArticleTitleRisk factors for recurrence after resection of hepatitis C virus-related hepatocellular carcinoma World J Surg 24 1559–65 Occurrence Handle10.1007/s002680010277 Occurrence Handle11193723

    Article  PubMed  Google Scholar 

  41. N Yamanaka M Takada T Tanaka J Yamanaka C Yasui T Ando et al. (2000) ArticleTitleViral serostatus and coexisting inflammatory activity affect metachronous carcinogenesis after hepatectomy for hepatocellular carcinoma. A further report J Gastroenterol 35 206–13 Occurrence Handle10.1007/s005350050332 Occurrence Handle10755690

    Article  PubMed  Google Scholar 

  42. MM Bilimoria GY Lauwers DA Doherty DM Nagorney J Belghiti KA Do et al. (2001) ArticleTitleUnderlying liver disease, not tumor factors, predicts long-term survival after resection of hepatocellular carcinoma Arch Surg 136 528–35 Occurrence Handle10.1001/archsurg.136.5.528 Occurrence Handle11343543

    Article  PubMed  Google Scholar 

  43. S Kubo H Tanaka T Shuto S Takemura T Yamamoto T Uenishi et al. (2004) ArticleTitleCorrelation between low platelet count and multicentricity of hepatocellular carcinoma in patients with chronic hepatitis C Hepatol Res 30 221–5 Occurrence Handle10.1016/j.hepres.2004.10.005 Occurrence Handle15589130

    Article  PubMed  Google Scholar 

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Kubo, S., Tanaka, H., Shuto, T. et al. Prognostic effects of causative virus in hepatocellular carcinoma according to the Japan integrated staging (JIS) score. J Gastroenterol 40, 972–979 (2005). https://doi.org/10.1007/s00535-005-1681-1

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  • DOI: https://doi.org/10.1007/s00535-005-1681-1

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